Patterns of speciation are similar across mountainous and lowland regions for a Neotropical plant radiation (Costaceae:Costus)

Abstract

Author Contributions: Study was designed by OMV, DLG and KMK. KMK curated the plant collection used for genomic sampling. OMV, DLG and KMK collected the data. Phylogenetic analyses were conducted by OMV. Species richness and topographic complexity analyses were conducted by BG; all other geographic and climatic analyses were conducted by DLG. Juarez (UCSC) for help with field collecting, and Edgardo Ortiz for assistance with the analysis of the transcriptomic data. All field research was conducted with appropriate collection permits in Costa Rica (M AbstractHigh species richness and endemism in tropical mountains are recognized as major contributors to the latitudinal diversity gradient. The processes underlying mountain speciation, however, are largely untested. The formation of steep ecogeographic gradients and the geographic isolation of populations by geological features are predicted to promote speciation in mountains relative to lowland regions. We evaluate these processes in a species-rich Neotropical genus of understory herbs, Costus, that range from the lowlands to montane forests. We test for an association between topography and species richness, infer a biogeographical history, and ask whether the contributions of niche divergence, geographical isolation, and pollination shifts differ between mountain-influenced and Amazonian sister pairs inferred from a 756-gene phylogeny. We find that species richness is highest in topographically complex regions and infer that early Costus ancestors diverged in Central America during a period of mountain formation in the last 3 My.We find evidence for climatic divergence, geographical isolation, and pollination shifts in general, but do not find significant differences in these factors between mountain-influenced and Amazonian sister pairs. We conclude that despite higher indices of climatic niche and species diversity in the mountains, speciation patterns in Costus appear similar across tropical lowland and mountainous regions.

The genetic mechanisms underlying the convergent evolution of pollination syndromes in the Neotropical radiation of Costus L.

“…Mellitophilous flowers are most often subtended by green, often leafy, bracts while ornithophilous flowers are subtended by bright red, orange, or yellow bracts. Previous phylogenetic studies have estimated multiple shifts in pollination syndromes during the evolution of Neotropical Costus, including shifts to mellitophilous pollination syndromes and subsequent regains of ornithophilous flowers (Specht, 2006;Salzman et al, 2015;Valderrama et al, 2020;Vargas et al, 2020), mainly through sympatric speciation events (André et al, 2016). These results suggest that shifts in traits leading to distinct pollination syndromes, together with reproductive isolation via reinforcement, may account for the rapid radiation observed in this Neotropical clade.…”

The genetic basis of floral mechanical isolation between two hummingbird‐pollinated Neotropical understorey herbs

“…We also test for alignment in the direction of QTL effects with each other and with the parental trait differences that would indicate adaptive pleiotropy and/or linkage that could promote the evolution and maintenance of floral mechanical isolation in this system. Multilocus phylogenetic data show that they are very recently diverged species, and part of a larger recent and rapid Neotropical species radiation (Vargas et al, 2020). The species are sympatric throughout much of Central and Northwestern South America, but the range of C. pulverulentus extends further north into Mexico and Cuba.…”

“…Here, we examine the genetic architecture underlying floral divergence between two species of spiral gingers (genus Costus) living in sympatry and sharing their primary hummingbird pollinator but placing pollen on either the bird's bill or forehead. Previous studies in this system have established pollinator identity and visitation rates, the close phylogenetic relatedness of the species, the high relative importance of floral trait divergence to overall reproductive isolation, and the extent of hybridization and introgression in sympatry (Kay, 2006;Kay & Schemske, 2003, 2008Surget-Groba & Kay, 2013;Vargas et al, 2020). Unlike most long-lived perennial tropical plants, Costus can be grown to flowering in large numbers in the glasshouse in order to use a QTL mapping approach.…”

“…The species are sympatric throughout much of Central and Northwestern South America, but the range of C. pulverulentus extends further north into Mexico and Cuba. The range of C. scaber extends farther south and east into the Amazon basin and coastal Brazil; however, recent phylogenetic evidence shows that South American C. scaber represents a different taxon (Vargas et al, 2020).…”

The Origins and Drivers of Neotropical Diversity

“…Speciation may increase with altitude (Weir 2006;Drummond et al 2012;Pouchon et al 2018;Quintero & Jetz 2018;Vasconcelos et al 2020), or under environmental perturbations, such as Andean orogenic activity (Weir 2006;Madriñán et al 2013;Lagomarsino et al 2016;Pouchon et al 2018;Quintero & Jetz 2018;Esquerré et al 2019;Vasconcelos et al 2020), or seasonal climatic variations (Simon et al 2009;Fouquet et al 2014;Pinto-Ledezma et al 2017;Igea & Tanentzap 2020). However, this view is not without controversy, as some studies found that past environmental changes did not affect diversification, and that there are similar diversification patterns among Neotropical regions (Smith et al 2014;Harvey et al 2020;Vargas et al 2020). Unfortunately, up to date, most studies investigating this question focus on long-term dynamics of particular clades or in continental Neotropical scale patterns at shallow evolutionary times, i.e.…”